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\begin{document}

\title{Musculoskeletal Misdiagnoses in Pediatric Patients with Spinal Tumors}



\author[1]{Aurora Dybedokken}%
\author[2]{René  Mathiasen}%
\author[3]{Henrik Hasle}%
\author[3]{Troels Herlin}%
\author[4]{Michael Thude Callesen}%
\author[4]{Søren Holm Hansen}%
\author[1]{Laura Hallundbæk Jensen}%
\author[1]{Jesper Amstrup}%
\author[1]{Søren  Hagstroem}%
\author[1]{Ninna Brix}%
\affil[1]{Aalborg Universitetshospital}%
\affil[2]{Rigshospitalet}%
\affil[3]{Aarhus Universitetshospital}%
\affil[4]{Odense Universitetshospital}%


\vspace{-1em}



  
  \date{May 24, 2024}


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\begin{abstract}
\textbf{Objective}: Childhood spinal tumors often present with
musculoskeletal symptoms, potentially causing a misdiagnosis and delays
in diagnosis and treatment. This study aims to identify, characterize,
and compare children with spinal tumors who had prior musculoskeletal
misdiagnoses to those without, analyzing clinical presentation,
diagnostic interval, and outcome. \textbf{Study design}: This
retrospective cohort study evaluated all children aged 0-14 years
diagnosed with a spinal tumor in Denmark from 1996 to 2018. The cohort
was identified through the Danish Childhood Cancer Registry, and the
registry data were supplemented with data from medical records. The
survival was compared using the Kaplan-Meier method. \textbf{Results}:
Among 58 patients, 57\% (33/58) recieved musculoskeletal misdiagnoses
before the spinal tumor diagnosis. Misdiagnoses were mostly non-specific
(64\%, 21/33), involving pain and accidental lesions, while 36\% (12/33)
were rheumatic diagnoses. The patients with prior misdiagnosis had less
aggressive tumors, fewer neurological/general symptoms, and 5.5 months
median diagnostic interval versus 3 months for those without a
misdiagnosis. Those with prior misdiagnoses tended to have a higher
5-year survival of 83\% (95\% CI 63-92\%) compared to 66\% (95\% CI
44-82\%) for those without (p=0.15) \textbf{Conclusion}: Less aggressive
spinal tumors may manifest as gradual skeletal abnormalities and
musculoskeletal symptoms without neurological/general symptoms, leading
to misdiagnoses and delays.%
\end{abstract}%



\sloppy


\textbf{Introduction}

Spinal cord tumors are rare tumors in children, with an estimated
incidence of 0.27 per 100,000. The most common presenting symptoms are
pain of the bony segment directly over the tumor, abnormal gait or
coordination difficulties, spinal deformity, focal motor weakness, and
sphincter dysfunction. Spinal tumors are one of the childhood tumors
most frequently presenting with musculoskeletal symptoms. A recently
published nationwide registry-based cohort study by our group, including
all children with cancer in Denmark over 23 years, identified a
musculoskeletal diagnosis prior to the diagnosis of cancer in one-fifth
of the children with spinal tumors. Symptoms among these patients were
often nonspecific pain and might mimic rheumatic diseases, which can
lead to misdiagnosis and diagnostic delay.

Non-specific musculoskeletal pain is frequent among children and
although the percentage of children with cancer among those sent to the
rheumatology department is low, up to 60\% of children with cancer
initially evaluated in the rheumatology department are misdiagnosed.
Hematological cancers are predominant in the literature evaluating
musculoskeletal misdiagnosis in childhood cancer, including only few
cases of spinal tumors.

Misdiagnoses imply a risk of diagnostic delay, and earlier studies have
found the diagnostic interval (time from first symptoms until diagnosis)
to be twice as long for childhood cancers with a musculoskeletal
misdiagnosis. Prompt diagnosis and treatment of pediatric spinal tumors
is of special importance, as diagnostic delay can lead to damage to the
spinal cord, which may inflict permanent neuronal dysfunction. Survivors
of spinal tumors face a high disease burden of long-term effects from
tumor and treatment, with substantial morbidity, markedly reducing their
quality of life.

The objective of this retrospective cohort study was to identify and
characterize the subgroup of children with spinal tumors having a prior
musculoskeletal misdiagnosis and evaluate any patterns or red flags.
Further, we compared the group with and without musculoskeletal
misdiagnosis in terms of clinical presentation, diagnostic interval, and
outcome.

\textbf{Methods}

\textbf{Study design}

We performed a nationwide, retrospective study including all consecutive
cases of Danish pediatric patients aged 0-14 years diagnosed with a
spinal tumor from January 1\textsuperscript{st}, 1996, to December
31\textsuperscript{st}, 2018. The cohort was identified from a
nationwide (population of 5.8 million) registry-based cohort study,
previously described in detail, using The Danish Childhood Cancer
Registry (DCCR). The DCCR includes all cases classified as neoplasms
according to the International Classification of Diseases, 10th edition
(ICD-10) (diagnoses DC00-DD48). The DCCR is linked to the Danish
National Patient Registry (DNPR), the National Pathology Registry, and
the Danish Cancer Registry using the unique national identification
number assigned to all permanent residents in Denmark at birth or
immigration.

\textbf{Data collection}

The registry data from DCCR were supplemented with data from medical
records from all pediatric departments in Denmark. To assess the impact
of a misdiagnosis on patient outcomes, we identified patients with a
prior musculoskeletal misdiagnosis and compared their characteristics to
the remaining patients without any musculoskeletal misdiagnosis. The
following data were collected: demographic information such as age and
gender, the clinical presentation (symptom, objective signs), the
diagnostic intervals, tumor type and grade, metastases, treatment,
comorbidities. We also collected data of cause and date of death, last
day of follow-up, and presence of sequelae from tumor or treatment.
Sequelae was categorized according to organ and severity, severe
sequelae included plegia, incontinens or neurocognitive defects.

The musculoskeletal diagnosis was recorded as a misdiagnosis if the
symptoms were later found to be due to the tumor. It was recorded as
musculoskeletal comorbidity if it was a coexisting musculoskeletal
diagnosis and the symptoms were not later explained by the tumor. The
diagnoses included were from hospitalizations, emergency room, and
outpatient visits but not from general practitioners.

We used a standardized definition of the diagnostic intervals, including
the period from the first symptom until the start of treatment. Further,
three additional time intervals were added: 1) a pre-diagnostic
symptomatic interval, i.e., the time from the first symptom until
diagnosis. 2) a first hospital doctor interval, i.e., the time from the
first hospital contact until a specialist was involved; and 3) a
specialist interval, i.e., the time from a specialist was involved until
the final diagnosis was made. The specialist was defined as either a
pediatric oncologist or neurosurgeon, (Fig. 1).

\textbf{Statistical analysis}

Categorical data were tabulated by prevalence, and Fisher's exact test
was used for comparisons. All continuous data were non-normally
distributed (evaluated by histograms and QQ-plots), and comparisons were
made by Mann-Whitney U-test and tabulated with median, interquartile
range (IQR) with lower quartiles as 25th percentile and upper quartiles
as 75th percentile and range. For mortality analysis, we followed
patients from the date of tumor diagnosis until death, emigration, or
the end of follow-up (October 1\textsuperscript{st}, 2022). The
Kaplan-Meier method was used to compare the one- and five-year survival
for the children with versus without a prior musculoskeletal
misdiagnosis. All statistical tests were performed under a two-sided
significance level of 0.05. STATA/MP 17.0 was used for the statistical
analysis.

The study was approved by the Danish Data Protection Agency (record
number 1-16-02-214-16). This study followed the Strengthening the
Reporting of Observational Studies in Epidemiology (STROBE) (reporting)
guidelines.

\textbf{Results}

According to the original cohort based on registry data, 87 patients
below 15 years were diagnosed with a spinal tumor in Denmark from
January 1\textsuperscript{st}, 1996 to December 31\textsuperscript{st},
2018.

17 patients were excluded due to misclassification, as they were not
classified as classical spinal tumors, being brain tumors, Langerhans
cell histiocytosis, lymphoma, hemangioma, hamartoma, sarcoma, and bone
sarcomas with location in the spinal cord. Further, 12 patients were
excluded due to missing records or insufficient data, (Fig. 2).

The final cohort of the present study included 58 patients aged 0-14
years diagnosed with a spinal tumor. 64\% (37/58) had a prior
musculoskeletal diagnosis, and 89\% (33) of these were a misdiagnosis.
Thereby a total of 57\% (33/58) had a musculoskeletal misdiagnosis. The
majority (64\%, 21/33) of the misdiagnoses were non-specific including
musculoskeletal pain (46\%, 16/33), and accidental musculoskeletal
lesions, often evaluated at the emergency room (15\%, 5/33) such as
torticollis, muscle strains, and sprains. A specific rheumatic
misdiagnosis occurred in 36\% (12/33) and included arthritis,
arthropathy, osteomyelitis, discitis, inflammatory spondylopathy,
reactive arthritis, and scoliosis.

In Table 1 we compare the clinical characteristics: age, gender, tumor
type, metastases, treatment, and comorbidities of the group with versus
without a musculoskeletal misdiagnosis. There was no difference in
gender distribution between the two groups. Patients with a prior
misdiagnosis were older (median age 10.5 vs. 5.9, p=0.04). Most of the
tumors were low-grade tumors, present in 82\% vs 68\% (p=0.35).
Ependymoma was the most common type of tumor in both groups (found in
27\% vs. 20\%, p=0.56). Low-grade astrocytoma was slightly more
prevalent in the group with a misdiagnosis (24\% versus 16\%, p = 0.53),
whereas high-grade astrocytoma, glioblastoma, medulloblastoma and
primitive neuroectodermal tumor (PNET) occurred more often in patients
without a misdiagnosis (32\% vs. 9\%, p=0.002), Table 1. Metastases to
the brain were less frequent in the group with a misdiagnosis (9 \% vs.
24\%, p=0.15). Additional treatment was less prevalent in patients with
a misdiagnosis: 21\% received steroids or pressure relieving operations
compared to 40\% of patients without a misdiagnosis (p=0.15), and only
15\% received chemotherapy compared to 40\% of the patients without
misdiagnosis, (p=0.04). Comorbidity occurred less frequent in patients
with a misdiagnosis compared to those without (39\% versus 60\%,
p=0.18), mainly due to a lower frequency of CNS comorbidity, including
epilepsy and mental retardation, present in 6\% with misdiagnosis and
24\% without (p=0.15), Table 1.

In Table 2, we present a comparison of the clinical presentation for the
group with versus without a misdiagnosis, with pain and paresis as the
most common presentation in both groups. Musculoskeletal symptoms were
present in 100\% of patients with a misdiagnosis versus 56\% of patients
without (p= \textless{} 0.001). In the patients with a misdiagnosis the
most common presenting symptom was localized pain in the lower limb,
neck, and/or back, occurring in 81\% compared to 28\% of the patients
without a misdiagnosis (p \textless{} 0.001), Table 2.

Neurological symptoms were less common in patients with a misdiagnosis
(63\%) compared to those without (96\%; p=0.004), (Table 2).
Furthermore, general symptoms such as fatigue, fever, and weight loss
were less frequent in patients with a misdiagnosis (21\% vs. 52\%,
p=0.02). Physical findings were highly prevalent and did not differ
between the two groups, with abnormal neurological findings,
particularly paresis, sensory deprivation, and disordered reflexes,
being the most frequent (Table 2).

Mistreatment in the form of physiotherapy, chiropractor or painkiller
occurred only among the patients with a misdiagnosis (36\%, p
\textless{} 0.001). Almost a third (27\%) of the misdiagnosed children
had received prior physiotherapy treatment. The time from first symptom
until evaluated at the hospital (parental and primary care interval) did
not differ compared to the cases not receiving physiotherapy, being
respectively 60 days (IQR 22; 540, range 0;788), compared to 59 days
(IQR 13; 100, range 3;730), p=0.34. Though, when comparing to the
patients without a misdiagnosis they have a shorter interval with 27
days (IQR 4;91, range 0-880), p=0.10.

Table 2 and Fig. 3, provide a comparison of diagnostic intervals for
patients with and without a misdiagnosis. Patients with a misdiagnosis
experienced a longer total interval (time from onset of symptoms until
treatment) with a median time of 165 days (IQR 35;318), compared to 97
days (IQR 28; 176) for those without a misdiagnosis (p=0.07), mainly due
to longer parental and primary care intervals. Half of the patients
(52\%) with a misdiagnosis had a total interval exceeding six months,
compared to one third (32\%) of patients without a misdiagnosis
(p=0.18).

The first hospital doctor was a pediatrician in 60\% of all cases.
However, for patients with a misdiagnosis, orthopedic doctors or general
doctors in the emergency room were the first hospital doctor in 21\% of
cases, compared to zero cases for patients without a misdiagnosis
(p=0.02). A referral to a specialist occurred after the tumor diagnosis
was established in 79\% of cases, resulting in a median specialist
interval of 0 days (IQR 0;1).

In order to further investigate any patterns or red flags in the group
with a musculoskeletal misdiagnosis we performed an analysis comparing
the 12 patients with a specific ``rheumatic'' misdiagnosis (including
arthritis, arthropathy, osteomyelitis, discitis, inflammatory
spondylopathy, reactive arthritis, and scoliosis) to the 21 patients
with a non-specific musculoskeletal misdiagnosis (including
musculoskeletal pain and accidental musculoskeletal lesions). Further
the 12 patients with specific ``rheumatic'' misdiagnosis were compared
to the 25 patients without a misdiagnosis, Supplemental Table S1. The
patients with a specific rheumatic misdiagnosis predominantly had
low-grade tumors (83\%), and metastasis did not occur in this group.
High-grade tumors occurred in respectively 17\% and 19\% of the children
with misdiagnoses and in 32\% of the children without musculoskeletal
misdiagnoses (p = 0.45). Pain as the first presenting symptom occurred
in 95\% of the patients with non-specific misdiagnoses compared to 42\%
in the group with specific rheumatic misdiagnoses (p\textless{}0.001).
The frequency of other symptoms and findings did not differ for the
children with specific versus non-specific misdiagnoses. When comparing
the diagnostic interval for these three subgroups we found an even
longer secondary care interval in the subgroup with a specific
misdiagnosis, including a long first hospital doctor interval of 128
days (IQR 13; 153), compared to 10 days (IQR 1; 74) for the subgroup
with non-specific misdiagnoses (p=0.10), and 7 days (IQR 1; 45) for the
group without a misdiagnosis (p=0.01).

The impact of a musculoskeletal misdiagnosis on overall survival is
illustrated in a Kaplan-Meier curve (Fig. 4). The group with a prior
misdiagnosis tended to have a higher 5-year survival of 83\% (95\% CI
63-92\%), compared to 66\% (95\% CI 44-82\%) for the patients without
musculoskeletal misdiagnoses (p=0.15). For the total cohort, 55\%
achieved complete remission and 25\% (15/58) died due to tumor or
treatment. The median duration of follow-up was 10.6 years (IQR 5.2;
14.7), being 8.8 years (IQR 7.1; 21.1) for children with misdiagnoses
and 11.3 (IQR 8.6; 12.6) years for the children without, p=0.45.

Sequelae were highly prevalent among all patients, reported in 63\% with
a misdiagnosis and 76\% of patients without a misdiagnosis (p=0.37).
Severe sequelae occurred in 42\% of patients with a misdiagnosis and
56\% of patients without (p=0.43). There was no significant difference
in the frequency of musculoskeletal sequelae when comparing the two
groups (24\% vs. 20\%, p=0.76). Similarly, there was no significant
difference in the frequency of central nervous system (CNS) sequelae
between the two groups (52\% vs. 60\%, p=0.60). The most frequent CNS
sequelae were paraplegia, paresis, sensory impairment, incontinence, and
decreased cognitive function.

\textbf{Discussion}

This study highlights a high prevalence of musculoskeletal misdiagnoses
among Danish children who were diagnosed with spinal tumors. In
two-thirds of children with spinal tumors, musculoskeletal misdiagnoses
were identified, resulting in a longer diagnostic interval compared to
children without musculoskeletal misdiagnoses. This subgroup of patients
frequently exhibited less aggressive tumors, rarely developed metastases
or required additional therapy beyond surgery and tended to have a
higher 5-year survival. These findings suggest that less aggressive
tumors can gradually manifest as skeletal abnormalities and
musculoskeletal symptoms without concurrent neurological or general
symptoms, thereby leading to misdiagnosis.

Physicians who evaluate children with musculoskeletal pain must always
consider the potential presence of an underlying tumor. Although it is
widely acknowledged that pediatric cancers are frequently misdiagnosed,
with rates ranging from 52-60\%, musculoskeletal misdiagnoses have
previously mainly been studied in children with hematological cancers.

Patients who were misdiagnosed with musculoskeletal conditions often
presented with localized pain in the lower limb, back, or neck,
accompanied by gait abnormalities and nocturnal pain. The literature
states pain as the most prevalent symptom of spinal tumors, followed by
motor weakness, sciatica, and sensory deficits. It is imperative to
approach any occurrence of new-onset, persistent, localized, and severe
pain in a previously asymptomatic child with utmost seriousness,
warranting thorough consideration of an underlying pathological
condition.

Despite medical advances, the diagnostic intervals are still very long
for spinal tumors. Multiple studies have revealed a median diagnostic
interval ranging from 2-8 months. In the presence of a misdiagnosis the
diagnostic interval for pediatric cancers is twice as long. To the best
of our knowledge, the present study is the first to investigate the
impact of a musculoskeletal misdiagnosis on the time intervals of
pediatric spinal tumors. Our results indicate that patients with a
musculoskeletal misdiagnosis have a significantly longer median total
interval of 5.5 months compared to 3 months for patients without a
misdiagnosis, primarily due to a longer parental and primary care
interval. In addition, the subgroup with a specific rheumatic
misdiagnosis had an even longer first hospital doctor interval, often
due to a delay after a visit to the emergency room. The median duration
was four months for this subgroup compared to one week for the children
without a musculoskeletal misdiagnosis (p=0.01).

Multiple studies have previously revealed associations that extend the
diagnostic interval (age, symptoms, and tumor grade, among others).
Koshimizu et al., conducted a study evaluating factors contributing to a
delay in the diagnosis of pediatric spinal tumors. They discovered
neurological symptoms as the presenting symptom was associated with
early diagnosis, and the symptom of pain in the lower limb or back was
associated with a longer duration of symptoms until diagnosis. They
recommended that children experiencing pain lasting more than one month
should undergo an MRI to exclude serious spinal disorders.

The present study found no association between longer time intervals and
decreased survival. Patients with a musculoskeletal misdiagnosis had the
highest 5-year survival rate. This is in accordance with most
literature. Bouffet et al., found that patients with a shorter symptom
duration (\textless{}2 months) had a poorer outcome than those with
longer symptom duration (\textgreater{}2 months).

Previous investigations of pediatric CNS tumors have identified tumor
type and grade as key factors influencing survival, rather than the
diagnostic interval. Crawford et al., found that patients with
high-grade malignant spinal tumors had a shorter duration of symptoms
and significantly poorer survival compared to patients with low-grade
tumors. In the present study, patients with a musculoskeletal
misdiagnosis frequently had less aggressive tumors, rarely developed
metastases or required additional therapy beyond surgery. Furthermore,
these patients demonstrated a tendency towards higher 5-year survival
rates. This may indicate that less aggressive tumors can provoke slowly
developing skeletal abnormalities and musculoskeletal symptoms without
neurological or general symptoms, causing misdiagnoses and diagnostic
delays.

Survivors of spinal tumors experience a considerable disease burden due
to long-term complications from both the tumor and it's treatment, which
markedly reduce their quality of life. In this study, sequelae were
highly prevalent in all patients, occurring in two-thirds of the cases,
consistent with literature, underscoring the significant impact spinal
tumors implicate on patients. Notably, the patients with a
musculoskeletal misdiagnosis did not demonstrate a higher prevalence or
severity of sequelae compared to those without a misdiagnosis. This is
consistent with some studies, while others have suggested that delayed
diagnosis leads to decreased long-term quality of life.

The strengths of this study include the population-based setting
including a non-selected cohort of all pediatric spinal tumor cases
diagnosed in Denmark over a long period of 23 years. The study's broad
representation of tumor morphologies reflects the general population.
The comprehensive data collection enabled a detailed analysis of the
clinical course of pediatric spinal tumors, providing valuable insights
into potential areas for improving the diagnostic process. Further, the
evaluation of the diagnostic intervals was strengthened by using a
standardized model with several subintervals, which increases the
generalizability of the results.

This study has some limitations that require cautious interpretation.
Firstly, pediatric spinal tumors are rare, leading to few cases and
small subgroups, which may limit the statistical precision. Secondly,
retrospective evaluation of the clinical presentation based on doctors'
notes from medical charts may introduce recall bias, particularly for
time intervals and symptoms. Thirdly, a potential methodological
limitation is the fact that the data does not include primary care and
presumably underestimates the number of preliminary musculoskeletal
misdiagnoses. Fourthly, the study did not record where in the health
system misdiagnoses occurred, which precludes a definitive determination
of a correlation between misdiagnosis and diagnostic delay. Lastly, 12
out of 70 (17\%) patients were excluded due to insufficient or missing
medical charts, which could affect our findings.

\textbf{Conclusion}

Misdiagnosis frequently occurs in children with spinal tumors who
exhibit musculoskeletal symptoms, leading to delayed diagnosis. This
subgroup of patients frequently exhibited less aggressive tumors, rarely
developed metastases or required additional therapy beyond surgery and
tended to have a higher 5-year survival. These findings suggest that
less aggressive tumors can give rise to gradually developing skeletal
abnormalities and musculoskeletal symptoms, without accompanying
neurological or general symptoms, thereby leading to misdiagnosis.



\textbf{Figure Legends}

\textbf{Figure 1.} An illustration of the time intervals from first
presenting symptom until the start of treatment.

\textbf{Figure 2.} Flow chart of the study population.

\textbf{Figure 3.} Diagnostic intervals (days) in the group with versus
without a musculoskeletal misdiagnosis.

\textbf{Figure 4:} Kaplan-Meier overall survival curves for the patients
with versus without a musculoskeletal misdiagnosis.\selectlanguage{english}
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\verb`Table 1.docx`  available at \url{https://authorea.com/users/695159/articles/683970-musculoskeletal-misdiagnoses-in-pediatric-patients-with-spinal-tumors}

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